Copein, 1983(4), pp. 918-932
Taxonomy and Phylogeny of the Higher Categories
of Cryptodiran Turtles Based on a Cladistic
Analysis of Chromosomal Data
John W. Bickham and John L. Carr
Karyological data are available for 55% of all cryptodiran turtle species including
members of all but one family. Cladistic analysis of these data, as well as con
sideration of other taxonomic studies, lead us to propose a formal classification
and phylogeny not greatly different from that suggested by other workers. We
recognize 11 families and three superfamilies. The platysternid and staurotypid
turtles are recognized at the familial level. Patterns and models of karyotypic
evolution in turtles are reviewed and discussed.
OVER the past 10 years knowledge of turtle
karyology has grown to such an extent
that the order Testudines is one of the better
known groups of lower vertebrates (Bickham,
1983). Nondifferentially stained karyotypes are
known for 55% of cryptodiran turtle species
and banded karyotypes for approximately 25%
(Bickham, 1981). From this body of knowledge,
as well as a consideration of the morphological
variation in the order, we herein present a gen
eral review of the cryptodiran karyological lit
erature and a discussion of the evolutionary re
lationships of the higher categories of
cryptodiran turtles. Although this paper focus
es on the Cryptodira (the largest suborder of
turtles), the Pleurodira also has been well stud
ied in terms of standard karyotypes (Ayres et
al., 1969; Gorman, 1973; Bull and Legler, 1980)
and a few have been studied with banding tech
niques (Bull and Legler, 1980).
Historical review of taxonomic relationships.—The
primary subdivisions of the order comprising
the turtles have undergone a great many name
changes and rearrangements over the last 100
years. Cope (1871) presented an arrangement
of the families into suborders which is still widely
accepted today. Until Cope, the subordinal and
suprafamilial classification of turtles was pri
marily based on differences in the digits among
the sea turtles, the aquatic turtles and/or the
terrestrial tortoises. Hoffman (1890) and Kuhn
(1967) present reviews of the early classifica
tions.
Cope recognized the currently widely ac
cepted suborders Cryptodira and Pleurodira.
Two major differences between these two sub
orders are in the plane of retraction of the neck
and the relationship between the shell and pel
vic girdle. In the cryptodires ("hidden-necked"
turtles), the neck is withdrawn into the body in
a vertical plane and the pelvis is not fused to
either the plastron or carapace, whereas in the
pleurodires ("side-necked" turtles) the pelvic
girdle is fused to both the plastron and carapace
and the neck is folded back against the body in
a horizontal plane. Cope's suborder Athecae
includes only the Dermochelyidae and is no
longer recognized. Most authors include the
Dermochelyidae among the Cryptodira (Gaffney, 1975a; Mlynarski, 1976; Wermuth and
Mertens, 1977; Pritchard, 1979).
A few authors recognize the Trionychoidea
(sensu Siebenrock, 1909) and/or the Chelonioidea (sensu Baur, 1893) at a suprafamilial
rank equivalent with the Cryptodira and Pleu
rodira (Boulenger, 1889;Lindholm, 1929; Mer
tens et al., 1934). The suborder Cryptodira is
used here in the sense of Williams (1950) and
subsequent authors and includes all living nonpleurodiran turtles.
The families of the suborder Cryptodira are
arranged in various superfamilies by several au
thors. The Testudinoidea, Chelonioidea and
Trionychoidea are superfamilies common to
most of the recent classifications (Williams, 1950;
Romer, 1966;Gaffney, 1975a; Mlynarski, 1976).
However, the limits of these taxa are not uni
formly agreed upon.
The non-trionychoid freshwater and land
cryptodiran turtles include the Chelydridae,
Kinosternidae, Dermatemydidae, Platysternidae, Emydidae and Testudinidae and are usu
ally placed in the Testudinoidea (Williams, 1950;
Romer,
1966). Gaffney (1975a) includes the
Kinosternidae and Dermatemydidae in the
© 1983 by the American Society of Ichthyologists and Herpetologists
BICKHAM AND CARR—TURTLE CHROMOSOME PHYLOGENY
Trionychoidea. Mlynarski (1976) includes only
919
ilies is difficult. The fact that a scale is in the
the Emydidae and Testudinidae in the Testu-
same position in members of different families
dinoidea. He recognizes the superfamily Che-
does not necessarily imply homology (Hutchi
lydroidea to include the Chelydridae, Derma-
son and Bramble, 1981).
temydidae, Kinosternidae and Platysternidae.
The Chelonioidea includes the Cheloniidae
Methods
and the Dermochelyidae (Baur, 1893; Gaffney,
1975a). Williams (1950), Romer (1966), and
Mlynarski (1976) recognize a separate superfamily, the Dermochelyoidea, for the family
Dermochelyidae, and include only the Cheloni
idae in the Chelonioidea.
Details for the procedures for turtle cell cul
ture, chromosome preparation, and banding
analysis have been published (Bickham, 1975;
Bickham and Baker, 1976a; Sites et al., 1979b).
Chromosomes were arranged, according to the
The Trionychoidea usually includes both the
Trionychidae and Carettochelyidae (Mlynarski,
1976), but Williams (1950) and Romer (1966)
recognize the Carettochelyidae separately in the
method of Bickham (1975), into three groups
Carettochelyoidea.
and group C microchromosomes. The A:B:C:
Most of the currently utilized family or
subfamily level taxa have been commonly rec
ognized since Boulenger (1889). However, there
formula is given after the diploid number in
is no complete agreement regarding the level
at which certain taxa should be recognized. Par
sons (1968) reviewed this confusing situation
with regard to the Chelydridae, Staurotypidae,
Kinosternidae, Platysternidae, Emydidae and
Testudinidae, as recognized here. Not men
tioned by him are the inclusion of Platysternon
in the Chelydridae (Agassiz, 1857; Gaffney,
1975b) and the recognition of the Staurotypi
dae (Baur, 1891, 1893; Chkhkvadze, 1970).
The above discussion of the history of cryptodiran taxonomy serves to illustrate the com
plexity of the relationships of the inclusive taxa.
The taxonomic confusion seems to result from:
analysis of (mostly) published data. In reanalyz
1) extensive convergent evolution in certain
morphological traits, 2) the failure of some
workers to distinguish between shared primi
tive and shared derived character states and 3)
the lack of a widely accepted phylogeny of tur
tles. Chromosomal data are used in this paper
in an attempt to solve some of the evolutionary
and classificatory problems. Cytogenetic infor
mation seems useful at this level because of the
high degree of conservatism expressed in chelonian karyotypes (Bickham, 1981). Addition
ally, the application of chromosome banding
techniques solves one of the most troublesome
problems in phylogeny reconstruction; namely,
(A:B:C:) where group A included metacentricsubmetacentric macrochromosomes, group B
subtelocentric-telocentric macrochromosomes,
Fig. 3 and in the text.
This paper represents a synthesis and re-
ing the data we employed cladistic methodology
(Hennig, 1966) in which sister groups were es
tablished by the determination of groups that
possessed shared derived characters (synapo-
morphies). Because banded karyotypes were not
available for the most appropriate outgroup
taxon (Suborder Pleurodira: Family Chelidae)
we employed an "internal" method of character
polarity determination. Specifically, characters
that were shared among families considered to
be distantly related, known from the fossil re
cord to be early derivatives of the cryptodiran
radiation, or thought to be morphologically
primitive, were considered as primitive (plesiomorphic) chromosomal characters. Because of
the nature of karyotypic variation in cryptodires
the analysis was rather straightforward. For ex
ample, dermatemydids are among the most
primitive living turtles and their fossil history
extends back to the Cretaceous, as does the che-
loniids which are thought to be an early offshoot
of the cryptodiran line. These two families pos
sess species with apparently identical karyo
types. It is highly unlikely that these two families
possess a synapomorphy at this level of the phy
logeny. This would mean that these two families
were more closely related to each other than to
the determination of homologous characters.
When two chromosomes have identical banding
patterns it can safely be concluded that they are
any other families studied, an arrangement that
homologous. It is sometimes difficult to deter
mine homology among morphological charac
sidered this karyotype to be primitive, at least
for the non-trionychoid families, and the karyo
appeared to conflict with every other line of
evidence in the literature. We therefore con
ters. For example, determination of homologies
types of other families were derived from this
among the plastral scales of various turtle fam
(see below).
920
COPEIA, 1983, NO. 4
*l
It*
#;*
MM
II 1!
B
ft*
#■#
Fig. 1.
G-band karyotype of a batagurine emydid (Chinemys reevesi, 2n = 52). The chromosomes are ar
ranged into group A (metacentric or submetacentric macrochromosomes), group B (telocentric and subtelocentric macrochromosomes), and group C (microchromosomes).
Results and Discussion
The following discussion is segmented into
the commonly accepted family groups. In gen
is unclear (Bickham and Baker, 1976a). There
is no karyotypic evidence to indicate emydines
are at all closely related to Rhinoclemmys, the
only New World batagurine genus (Carr, 1981).
eral, we have accepted each of the families as
There may be some hint of the batagurine-emy-
distinct entities and do not question their valid-
dine transition in the finding of several species
ity.
of Asiatic batagurines with 2n = 50 (Table 1).
Any relationship of the emydines to the 2n =
Emydidae.—The two subfamilies of emydid tur
50 batagurines will require evidence from other
tles are characterized by different karyotypes.
character systems in order to establish its exis
The predominantly New World emydines have
tence.
2n = 50 and the predominantly Old World batagurines mostly have 2n = 52 (Table 1). A few
Testudinidae.—The karyology of this family is
batagurine species also possess 2n = 50 (Table
not as well studied as that of the Emydidae but
it seems certain that the primitive karyotype is
1), including Siebenrockiella crassicollis, the only
emydid known to possess sex chromosomes (Carr
2n = 52. Some species are known to possess G-
and Bickham, 1981). Bickham and Baker (1976a)
band patterns identical to those of certain ba
concluded that the primitive karyotype of the
tagurines including Geochelone pardalis, G. elon-
Emydidae was 2n = 52 and identical to that of
gata and G. elephantopus (Dowler and Bickham,
Sacalia bealei and other Old World batagurines.
1982). C-band variation exists among species of
This has been supported by recent findings that
Geochelone,
some testudinids have banded karyotypes iden
species differ from Geochelone species by the
and
the
karyotypes
of Gopherus
tical to those of Chinemys reevesi and other ba
morphology and location of the nucleolar or
tagurines (Dowler and Bickham, 1982). Fig. 1
ganizing region (NOR) (Dowler and Bickham,
illustrates the karyotype of a batagurine (Chi
1982). Although this family is nearly world-wide
nemys reevesi) that possesses the proposed prim
in distribution and morhpologically diverse, the
itive emydid karyotype.
available data indicate a high degree of karyo-
The origin of the 2n = 50 emydine karyotype
logical conservatism.
BICKHAM AND CARR—TURTLE CHROMOSOME PHYLOGENY
Table 1.
921
Diploid Numbers of Cryptodiran Turtles. Each reference is listed under the currently rec
ognized name if different from that under which it was originally reported. Unpublished data have been
processed in our lab.
Taxon
Diploid
number
Source
Matthey,
1930,
1931; Wickbom, 1945; Polli,
1952; Matthey and Van Brink, 1957; Van
Brink, 1959; Ivanov, 1973
Van Brink, 1959; Forbes, 1966; Killebrew, 1977a
Glascock, 1915; Van Brink, 1959; Forbes, 1966;
Stock, 1972; DeSmet, 1978
Forbes, 1966
Jordan, 1914; Forbes, 1966
Forbes, 1966; Stock, 1972; Bickham and Baker,
1976a; Killebrew, 1977a
DeSmet, 1978
Stock, 1972
Killebrew, 1977a
DeSmet, 1978
Forbes, 1966; Gorman, 1973; Bickham and Bak
er, 1979
Forbes, 1966
Killebrew, 1977a
Stock, 1972; unpublished
Killebrew, 1977a
Gorman, 1973
Gorman, 1973; Killebrew, 1977a
Gorman, 1973; Bickham and Baker, 1976a, b,
1979
Bickham and Baker, 1976a, b
Unpublished
Bickham and Baker, 1976a, b
Forbes, 1966; McKown, 1972; Killebrew, 1977a
Forbes, 1966; Stock, 1972; Bickham and Baker,
1979
Forbes, 1966; McKown, 1972
McKown, 1972; Killebrew, 1977a
McKown, 1972; Stock, 1972; Killebrew, 1977a
McKown, 1972
Killebrew, 1977a
McKown, 1972
McKown, 1972; Unpublished
McKown, 1972; Killebrew, 1977a
McKown, 1972; Killebrew, 1977a
McKown, 1972; Killebrew, 1977a
McKown, 1972; Killebrew, 1977a
Stock, 1972; Bickham and Baker, 1976a; Kille
brew, 1977a
COPEIA, 1983, NO. 4
922
Table 1.
Continued.
Diploid
Taxon
T. Carolina
number
[32]*
50
Source
Jordan, 1914
Forbes, 1966; Huang and Clark, 1967; Clark et
al., 1970; Stock and Mengden, 1975; Bickham
and Baker, 1979
T. c. triunguis
50
Forbes, 1966; Stock, 1972; Killebrew, 1977a
T. coahuila
50
Killebrew, 1977a
Deirochelys reticularia
50
Stock, 1972; Killebrew, 1977a
D. r. chrysea
50
Forbes, 1966
Malaclemys terrapin
50
Forbes, 1966; Stock, 1972
M. L littoralis
50
McKown, 1972
Emydoidea blandingi
50
Forbes, 1966; Stock, 1972
Clemmys insculpta
48
Forbes, 1966
50
Stock, 1972; Bickham, 1975, 1976
48
Forbes, 1966
50
Stock, 1972; Bickham, 1975
C. m. marmorata
50
Stock, 1972; Bickham, 1975
C. m. pallida
50
Killebrew, 1977a
C. muhlenbergi
50
Bickham, 1975
52
Bickham, 1975; Bickham and Baker, 1976a
C. guttata
BATAGURINAE
Sacalia bealei
50
Killebrew, 1977a
52
Bickham, 1975, 1976
M. c. rivulata
52
Bickham, 1975, 1976
M. mutica
52
Nakamura, 1935, 1937,1949; Stock, 1972; Gor
M. japonica
52
Nakamura, 1935; Sasaki and Itoh, 1967; Becak
Mauremys caspica leprosa
man, 1973; Bickham, 1975; Killebrew, 1977a
et al., 1975
Bickham and Baker, 1976a, b
Barros et al., 1975; Bickham and Baker,
1976a, b
Killebrew, 1977a
Killebrew, 1977a; Carr, 1981
Carr, 1981
Carr, 1981
Nakamura, 1937, 1949
DeSmet, 1978; Carr, 1981
DeSmet, 1978
Sasaki and Itoh, 1967, Takagi and Sasaki, 1974;
Killebrew, 1977a; Sites et al., 1979a; Dowler
and Bickham, 1982; Haiduk and Bickham,
1982
Gorman, 1973
Nakamura, 1949; Stock, 1972; Killebrew, 1977a;
DeSmet, 1978; Haiduk and Bickham, 1982
Carr, 1981
Gorman, 1973
BICKHAM AND CARR—TURTLE CHROMOSOME PHYLOGENY
Table 1.
Taxon
923
Continued.
Diploid
number
Source
C. flavomarginata
Kachuga tecta
K. smithi
K. trivittata
K. dhongoka
Ocadia sinensis
Malayemys subtrijuga
Orlitia borneensis
Siebenrockiella crassicollis
Callagur borneoensis
Hieremys annandalei
TESTUDINIDAE
Gopherus agassizi
52
Atkin et al., 1965; Ohno, 1967, 1971; Huang
and Clark,
1969; Jackson and Barr, 1969;
Stock, 1972; Gorman, 1973
G. berlandieri
52
Stock,
1972;
Gorman,
1973;
Killebrew and
McKown, 1978; Dowler and Bickham, 1982
G. polyphemus
54
Forbes, 1966
52
Dowler and Bickham, 1982
Kinixys belliana belliana
52
Killebrew and McKown, 1978
Testudo hermanni
52
Stock, 1972
T. graeca
52
Huang and Clark, 1969; Clark etal., 1970; Shindarov et al., 1976
54-60
Geochelone denticulata
52
Matthey, 1930
Sampaio et al., 1969, 1971; Bickham, 1976;
Bickham and Baker, 1976a, b
Forbes, 1966; Sampaio etal., 1971; Stock, 1972;
Bickham and Baker, 1976b
Unpublished
Goldstein and Lin, 1972; Benirschke et al., 1976;
Dowler and Bickham, 1982
DeSmet, 1978; Dowler and Bickham, 1982
Dowler and Bickham, 1982
Benirschke et al., 1976
Dowler and Bickham, 1982
Gorman, 1973; Haiduk and Bickham, 1982
Bull et al., 1974; Moon, 1974
Gorman, 1973
Bull et al., 1974; Moon, 1974; Killebrew, 1975
924
COPEIA, 1983, NO. 4
Table 1.
Taxon
S. salvini
Continued.
Diploid
number
Source
56
Gorman, 1973
54
Bull et al., 1974; Moon, 1974; Sites et al.,
1979a, b
CHELYDRIDAE
Chelydra s. serpentina
52
Forbes, 1966; Stock, 1972; Gorman, 1973; Bick
ham and Baker,
DeSmet, 1978
C. s. os ceo I a
C. s. acutirostris
Mac rod em ys tern m inckii
KINOSTERNIDAE
Kinosternon flavescens
K. sub rub rum
K. s. hippocrepis
K. s. steindachneri
K. leucostomum
K. I. postinguinale
K. hirtipes
K. integrum
K. herrerai
K. scorpioides
K. s. scorpioides
K. s. carajasensis
K. s. abaxillare
K. s. cruentatum
K. bauri
Sternotherus odoratus
S. carinatus
S. minor
DERMATEMYDIDAE
Dermatemys mawii
CHELONIIDAE
Caretta caretta
Chelonia my das
Eretmochelys imbricata
1976a; Killebrew,
1977b;
BICKHAM AND CARR—TURTLE CHROMOSOME PHYLOGENY
Table 1.
925
Continued.
* Reported as N = 16.
Platysternidae.—The standard karyotype of the
single species of platysternid (Platysternon meg
acephalum) has 2n = 54 (Haiduk and Bickham,
1982). This species appears to have close affin
ities to the Emydidae but is karyotypically dis
tinct from all emydids thus far studied. Because
P. megacephalum and emydids do apparently have
synapomorphic chromosomes that are not
shared with chelydrids, Haiduk and Bickham
(1982) considered P. megacephalum to comprise
a family distinct from the Chelydridae (sensu
Gaffney, 1975b) and resurrected the Platyster
nidae (Gray, 1870), a move also suggested by
Whetstone (1978).
element in emydids and testudinids (and platysternids based on standard chromosome mor
phology). This chromosome is acrocentric in
chelydrids, kinosternids, dermatemydids and
cheloniids (Fig. 2). We conclude that the biarmed
condition is derived. Centric fusion of the an
cestral acrocentric macrochromosome with a
microchromosome accounts for the presence of
a subtelocentric macrochromosome in the com
mon ancester of the Emydidae, Testudinidae,
Platysternidae and Staurotypidae. This is indic
ative of the staurotypids belonging to a clade
that does not include kinosternids (Kinosternon
and Sternotherus). This seems irreconcilable with
Staurotypidae.—This group is usually consid
ered to be a subfamily (Staurotypinae) of the
Kinosternidae. Standard karyotypes of all three
species in this group are known (Table 1; see
especially Bull et al., 1974). The two species of
Staurotypus are distinctive in possessing an XX/
XY sex chromosome system (Bull et al., 1974;
Sites et al., 1979a). Claudius angustatus, like
nearly all other turtle species studied, does not
possess heteromorphic sex chromosomes but
appears to be otherwise karyotypically identical
to Staurotypus (Bull et al.,
1974). Sites et al.
(1979a, b) report banded karyotypes of 5. sal-
Fig. 2.
G-band patterns of the second group B
chromosomes of (left to right) a staurotypid, an emydid, a kinosternid and a cheloniid. The long arms of
all 4 taxa are identical; the short arms of the stau
rotypid and emydid are euchromatic and identical,
vini and show that this species possesses a
biarmed second group B macrochromosome
cheloniid are small and heterochromatic; see text for
that appears to be homologous to an identical
further discussion.
however, the short arms of the kinosternid and the
926
COPEIA, 1983, NO. 4
the current classification; it is therefore pro
stantiated by recent studies using current tech
posed that the Staurotypinae be elevated to fa
niques.
milial rank.
Trionychidae.—Members
of both
subfamilies
Chelydridae.—The two extant species of this
family have been studied for both standard (Ta
ble 1) and banded karyotypes (Haiduk and Bickham, 1982). Chelydra serpentina and Macroclemys
temminckii both have 2n = 52 but differ in the
morphology of certain chromosomes. Haiduk
cation of this specimen (Kachuga dhongoka, Em-
and Bickham (1982) conclude that these two
ydidae; Singh, 1972). The 2n = 66 karotype was
species do not share any derived chromosomal
characteristics with each other or with any oth
primitive karyotype for the family. Banding
er families of Cryptodira. However, the karyo-
comparisons between Trionyx and Chelonia re
(Cyclanorbinae and Trionychinae) have 2n =
66 (Table 1). Reports of other diploid numbers
have been unsubstantiated in subsequent stud
ies. The report of 2n = 52-54 in Trionyx leithii
(Singh et al., 1970) was due to the misidentifi-
considered by Bickham et al. (1983) to be the
type of M. temminckii could be derived from that
vealed little homology between the Trionychi
of C. serpentina. The latter is considered the
dae and Cheloniidae (Bickham et al., 1983).
primitive karyotype for the family.
Carettochelyidae.—The
single
extant
species
Kinosternidae.—This family is comprised of two
(Carettochelys insculpta) has 2n = 68 (Bickham et
genera and about 18 species and has been well
al., 1983). Although no banding data have been
studied karyotypically (Table 1). Early, and ap
reported for this species, the standard karyo
parently inaccurate, reports aside (Table 1), all
type is very similar to the 2n = 66 karyotype of
species thus far examined appear to possess
trionychids.
2n = 56. Banded karyotypes (Bickham and Bak
er, 1979; Sites et al., 1979b) indicate all species
Taxonomy.—The acceptability of using karyo-
possess a large, subtelocentric macrochromo-
typic data in order to draw phylogenetic infer
some not found in any other group of turtles.
Kinosternids do not share any derived chro
mosomal characters with any other turtle fam
ily, including the staurotypids with which they
ences and erect a classification at the level of
are usually considered confamilial. An interest
acters and character states which may be pre
ing variation was found in this family by Sites
sumed to be closely enough related to be within
etal. (1979b). Heterochromatin that stains dark
the realm of influence of the same set of evo
in both G- and C-band preparations was found
lutionary constraints. According to this line of
in Sternotherus minor, Kinosternon baurii and K.
resasoning then, karyotypic data constitute a
subrubrum, but not found in K. scorpioides. The
character system separate from the character
presence of this type of heterochromatin was
systems associated with electrophoretic data or
considered to be a derived character (it is not
cranial osteology, etc. The level at which char
found in closely related families) shared among
acters are relatively constant within a group is
the three species that possess it, indicating that
the point at which those characters are of sys
family and higher is based upon the conserva
tism of the karyotypic character system. By
character system, we refer to a suite of char
the genus Sternotherus has affinities with tem
tematic utility and those characters are said to
perate species of Kinosternon.
be conservative (Farris, 1966). Our studies and
a review of the pertinent literature indicate that
Dermatemydidae.—The single extant species of
family level groups within the Cryptodira are
this family (Dermatemys mawii) possesses 2n = 56
(Table 1). There are no uniquely derived ele
characteristically karyotypically homogeneous
ments and this species shares no derived chro
logenetic sense) is observable interfamilially. It
mosomes with any other family.
and that the significant variation (in the phy
is upon these premises that we propose the clas
sification in Table 2 based upon our cladistic
Cheloniidae.—Members of this family possess
analysis of the karyotypic data.
2n = 56 (Table 1). Banding data indicate che-
This classification is conservative in that all
loniids and dermatemydids are karyotypically
families commonly recognized are maintained,
indistinguishable (Bickham et al., 1980; Carr et
even though in two instances there are family
al., 1981). Early reports of other diploid num
pairs which we cannot karyotypically distin
bers and sex chromosomes have not been sub
guish [i.e., Cheloniidae-Dermatemydidae and
BICKHAM AND CARR—TURTLE CHROMOSOME PHYLOGENY
Table 2.
927
Taxonomic Arrangement of the High
er Categories of Cryptodiran Turtles.
Suborder Cryptodira
Superfamily Chelonioidea
Family Cheloniidae
Family Dermochelyidae
Superfamily Testudinoidea
Family Emydidae
Family Testudinidae
Family Platysternidae
Family Staurotypidae
Family Chelydridae
Family Kinosternidae
Fig. 3.
Family Dermatemydidae
Cladogram showing the hypothesized re
lationships of the higher categories of cryptodiran
Superfamily Trionychoidea
turtles. The diploid number and the number of chro
Family Trionychidae
mosome pairs in groups A:B:C (Fig. 1) in the proposed
Family Carettochelyidae
primitive karyotype of each family (and both subfam
ilies of Emydidae) are shown. Because the trionychoid
families are so divergent, the A:B:C formulas are not
Testudinidae-Emydidae (in part)]. The classifi
cation departs from those that are commonly
given (Bickham et al., 1983). Characters 1 -5 are listed
and discussed in the text.
accepted in several respects, two of which de
serve further attention. The first is the removal
of the Dermatemydidae and Kinosternidae (plus
to recognize the Staurotypinae as a separate
Staurotypidae as herein conceived) from the
family, the Staurotypidae. This conclusion is in-
Trionychoidea
congruent with data from other character sys
(sensu
GafFney,
1975a).
Al
though Gaffney (197 5a) and Zug( 1971) present
tems. Many morphological studies report sim
morphological evidence for a relationship be
ilarities
tween these groups, the karyotypic evidence
Staurotypidae (among these Williams,
between
the
Kinosternidae
and
1950;
clearly indicates that these groups are from lin
Parsons, 1968; Zug, 1971). Most such studies
eages which have been separated for a long pe
have not attempted cladistic analyses (two ex
riod of time. No karyotypic apomorphies are
ceptions are Gaffney,
shared between the Trionychoidea, and the
Bramble, 1981). There seems no obvious or
Dermatemydidae and Kinosternidae and in fact
simple manner in which to reconcile the con
few symplesiomorphies remain (Bickham et al.,
flicting data from the karyotypic character sys
tem and the overwhelming amount of data from
various morphological character systems. In
1983;Carretal., 1981).
The Staurotypidae as herein recognized de
serves special attention. The karyotypic data
1975; Hutchison and
clearly indicate not only a relatively large karyo
recognizing the Staurotypidae, we have made
explicit our prediction of its relationships to
typic distance between the commonly recog
other testudinoid families. Independent confir
nized Kinosterninae and Staurotypinae, but also
mation or refutation of these relationships will
determine the merit of this move.
a clearly identifiable difference in direction of
karyotypic evolution in that the Staurotypidae
The three superfamilies are all considered to
can be allied synapomorphically in a derived
be holophyletic. Fig. 3 presents a cladogram
clade which does not include the Kinosternidae.
that we believe best reflects the branching se
Even if a karyotypic convergence on the apo-
quence of the evolution of this group. The Tes
morphic character allying the Staurotypidae
tudinoidea
with
groups but this is as yet unproved. The primi
the
Platysternidae,
Testudinidae,
and
Emydidae has occurred, the fact remains that
and
Chelonioidea
may be sister
tive karyotypes of these two taxa are identical,
the Kinosternidae and Staurotypidae would still
2n = 56 (character 1 in Fig. 3), and very differ
be karyotypically distinct (and nonrelatable), at
ent from that of the Trionychoidea, 2n = 66-
least to as great a degree as are any of the other
68 (character 2 in Fig. 3), but we do not yet
families. In the context of this paper and our
know the polarity of these character states
data-base we are left with no recourse except
(Bickham et al., 1983).
928
COPEIA, 1983, NO. 4
Platysternidae, Testudinidae, and Emydidae can
didae in the Trionychoidea (Gaffney, 1975a).
The chromosomal data do not support such an
arrangement because of the disparity in diploid
number and chromosome morphology between
testudinoids (including kinosternids and der
be identified by the presence of a biarmed sec
matemydids) and trionychoids (Bickham et al.,
ond group B macrochromosome (character 3
1983).
All testudinoid and chelonioid turtles possess
at
least
seven
group
A
macrochromosomes
(character 1 in Fig. 3). Among the testudinoid
families, a clade that includes Staurotypidae,
in Fig. 3; Fig. 2). Another clade includes the
Platysternidae, Testudinidae and Emydidae all
Chromosomal evolution.—We conclude, for two
of which primitively possess nine group A mac
reasons, that the primitive karyotype of the sub
rochromosomes (Fig. 1; character 4 in Fig. 3).
order Cryptodira is most likely the 2n = 56
A clade including the Emydidae and Testudin
karyotype of cheloniid and dermatemydid tur
idae is characterized by a 2n = 52 9:5:12 prim
tles. First, these are among the most ancient
itive karyotype (Fig. 1; character 5 in Fig. 3).
families in the suborder (both date from the
Species of the emydid subfamily Emydinae all
Cretaceous), and second, this karyotype is high
possess a karyotype derived from the primitive
ly generalized and could have given rise to the
9:5:12
diversity of karyotypes in the suborder by a min
arrangement
(Bickham
1976a).
The Dermatemydidae,
and
Baker,
imum number of events. A primitive karyotype
Kinosternidae
and
more similar to that of trionychoid turtles (2n =
Chelyridae possess no chromosomal synapo-
66-68) cannot entirely be ruled out (Bickham
morphies and the branching sequence of these
et al., 1983). Comparisons with karyotypes of
families is not obvious from chromosomal, mor
the species of Pleurodira do not solve the prob
phological or serological data. However, the
lem because species of the Chelidae are known
Chelydridae is usually considered to be most
to possess diploid numbers in the 2n = 56 range
closely related to the Emydidae (McDowell,
as well as the 2n = 66 range (Bull and Legler,
1964; Zug, 1971;Frair, 1972; Haiduk and Bick
1980). However, the primitive karyotype of the
ham, 1982) and the dermatemydids, morpho
Pleurodira was considered by Bull and Legler
logically one of the most primitive families of
(1980) to be 2n = 50-54 which is consistent with
turtles, are considered closely allied to the Kin
our hypothesis of a 2n = 56 ancestral karyotype
osternidae (Zug, 1971; Frair, 1972; Gaffney,
for the Cryptodira.
1975b).
The Cheloniidae and Dermochelyidae are
mosomal evolution in the Trionychoidea in
considered to comprise the suborder Chelo-
volved an increase in the diploid number by a
nioidea. There are no karyotypic data available
for Dermochelys coriacea so the relationship be
tween this species and cheloniids has yet to be
tested chromosomally. But, these two families
If the above hypothesis is true, then chro
reduction in the number of macrochromosomes
and an increase in the number of microchro-
mosomes. However, chromosomal evolution in
the Testudinoidea reduced the diploid number
are closely related morphologically and serologically (Frair, 1979). We follow most other
by an increase in the number of macrochro
workers in giving this group full superfamilial
crochromosomes.
mosomes and reduction of the number of mi-
status, recognizing that they have invaded an
Bickham and Baker (1979) note that species
adaptive zone, the marine environment, that is
within a family or subfamily possess identical or
distinctly different from that of most other tur
tles. It must be emphasized that Chelonia mydas
comparisons among families and subfamilies al
very similar karyotypes. However, karyotypic
(Chelonioidea) and Dermatemys mawii (Testudi-
most always reveal variation. A more refined
noidea) appear karyotypically identical and we
analysis of the pattern of karyotypic variation
interpret this to be the primitive karyotype of
in turtles (Bickham, 1981) suggests that the rate
these two superfamilies.
of karyotypic evolution has decelerated and that
The superfamily Trionychoidea includes only
Mesozoic turtles evolved at a rate twice as fast
the Trionychidae and Carettochelyidae. These
as their descendants. Additionally, the kinds of
two taxa are closely related chromosomally as
chromosomal rearrangements incorporated
well as morphologically and their karyotypes
during the diversification of cryptodiran fami
are distinctly different from those of species of
lies differ from the kinds of rearrangements in
the other two superfamilies. Some workers have
corporated during the evolution of modern
included the Kinosternidae and Dermatemy
species.
BICKHAM AND CARR—TURTLE CHROMOSOME PHYLOGENY
929
The above described pattern of karyotypic
often are found in isolated stock tanks, ponds,
evolution is consistent with the canalization
intermittent streams and permanent springs.
model of chromosomal evolution (Bickham and
Population sizes are often small and there is
Baker, 1979). Under this model, evolution of
probably very little migration among popula
the karyotype is driven by natural selection be
tions.
cause the chromosomal rearrangements alter
Many of the above mentioned biological char
genetic regulatory systems. Changes that are
acteristics of turtles conceivably could promote
adaptive accumulate more rapidly during the
chromosomal speciation. That it does not occur
early radiation of a lineage. As time goes on
in a major radiation (Cryptodira) does not mean
more and more adaptive linkage groups are
that the process is not viable in other taxa, but
produced.
Further
chromosomal
rearrange
its absence is somewhat unexpected. In conclu
ment tends to break up adaptive gene sequences
sion, population parameters are poorly corre
and the rate of chromosomal evolution slows
lated with chromosomal variability in turtles and
down. Thus, in an ancient group such as turtles,
in principle we agree with the criticisms of the
the process of canalization has had such a long
chromosomal speciation models espoused by
period of time to act that karyotypic evolution
Bickham and Baker (1979, 1980) and Futuyma
among modern forms is virtually nonexistent.
and Mayer (1980).
However, when karyotypic comparisons are
made of taxa that diverged early during turtle
evolution, such as comparisons of the primitive
karyotypes of families, variation is found to be
more pronounced.
Acknowledgments
Our work on turtle karyology has been fund
ed by the National Science Foundation under
Models that explain karyotypic evolution by
grants DEB-7713467 and DEB-7921519. We
population demography, such as deme size, do
are grateful to the numerous people who have
not apply to turtles. The classical model of chro
provided us with technical assistance, or spec
imens used in our analyses, including: T. W.
mosomal speciation (White, 1978) requires fix
ation of chromosomal rearrangements in small
Houseal, K. Bjorndal, E. O. Moll, F. L. Rose,
demes due to genetic drift or inbreeding. There
J. M. Legler,J.J. Bull, R. C. Dowler and M. W.
is some question as to whether chromosomal
Haiduk. Instructive comments on the manu
speciation is in fact a viable process (Bickham
script were received from D. M. Bramble, J. H.
and Baker, 1979, 1980; Futuyma and Mayer,
Hutchison and J. M. Legler.
1980), but even if it is, it certainly is not oper
ative in turtles. There are no known chromo
somal races in turtles. This could be explained
by turtles characteristically not having small
population sizes or other demographic factors
that promote the fixation of chromosomal rear
rangements by
genetic drift
or
inbreeding.
However, turtles display such a diversity of de
mographic
characteristics
(Auffenberg
and
Iverson, 1979; Bury, 1979; Bustard, 1979) that
this explanation seems untenable.
Turtles exhibit a diverse array of morpho
logical types and occur in nearly all habitats
available to reptiles. Some, such as the migra
tory sea turtles, are highly vagile but others,
such as tortoises, have relatively low vagility.
Reproductive rates also vary. The green turtle
may lay as many as 200 eggs in a single clutch,
some emydids may lay only a single large egg.
While there are certainly many species that
characteristically have large population sizes, we
can point to many that probably do not. For
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Department of Wildlife and Fisheries Sci
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College
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1982.